Quantitative morphology of the vascularisation of organs: A stereological approach illustrated using the cardiac circulation

Annals of Anatomy

Volumn 196, Issue 1, 2014, Pages 12-19

  Mühlfeld, Christian ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Arteries; Capillaries; Design based stereology; Heart; Vasculature; Veins

Indexed keywords

ARTERIES; CAPILLARIES; DESIGN-BASED STEREOLOGY; HEART; VASCULATURE; VEINS;

ANIMALS; CELL COUNT; CORONARY CIRCULATION; HEART; HUMANS; IMAGING, THREE-DIMENSIONAL; MICROSCOPY;

EID: 84895074378     PISSN: 09409602     EISSN: 16180402     Source Type: Journal    
DOI: 10.1016/j.aanat.2012.10.010     Document Type: Review

References (72)

1. Amann K., Gharehbaghi H., Stepfen S., Mall G. Hypertrophy and hyperplasia of smooth muscle cells of small intramyocardial arteries in spontaneously hypertensive rats. Hypertension 1995, 25:124-131.
2. Amann K., Törnig J., Buzello M., Kuhlmann A., Gross M.L., Adamczak M., Buzello M., Ritz E. Effect of antioxidant therapy with dl-α tocopherol on cardiovascular structure in experimental renal failure. Kidney Int. 2002, 62:877-884.
3. Anversa P., Olivetti G., Loud A.V. Morphometric study of early postnatal development in the left and right ventricular myocardium of the rat. I. Hypertrophy, hyperplasia, and binucleation of myocytes. Circ. Res. 1980, 46:495-502.
4. Anversa P., Capasso J.M., Ricci R., Sonnenblick E.H., Olivetti G. Morphometric analysis of coronary capillaries during physiologic myocardial growth and induced cardiac hypertrophy: a review. Int. J. Microcirc. Clin. Exp. 1989, 8:353-363.
5. Bassien-Capsa V., Fouron J.C., Comte B., Chorvatova A. Structural, functional and metabolic remodeling of rat left ventricular myocytes in normal and in sodium-supplemented pregnancy. Cardiovasc. Res. 2006, 69:423-431.
6. Batra S., Rakusan K. Geometry of capillary networks in hypertrophied rat heart. Microvasc. Res. 1991, 41:29-40.
7. Batra S., Rakusan K. Geometry of capillary networks in volume overloaded rat heart. Microvasc. Res. 1991, 42:39-50.
8. Boudoulas H., Rittgers S.E., Lewis R.P., Leier C.V., Weissler A.M. Changes in diastolic time with various pharmacologic agents. Implication for myocardial perfusion. Circulation 1979, 60:164-169.
9. Brinks H., Tevaearai H., Mühlfeld C., Bertschi D., Gahl B., Carrel T., Giraud M.N. Contractile function is preserved in unloaded hearts despite atrophic remodeling. J. Thorac. Cardiovasc. Surg. 2009, 137:742-746.
10. Brüel A., Nyengaard J.R. Design-based stereological estimation of the total number of cardiac myocytes in histological sections. Basic Res. Cardiol. 2005, 100:311-319.
11. Brüel A., Oxlund H., Nyengaard J.R. The total length of myocytes and capillaries, and total number of myocyte nuclei in the rat heart are time-dependently increased by growth hormone. Growth Horm. IGF Res. 2005, 15:256-264.
12. Charnock-Jones D.S., Kaufmann P., Mayhew T.M. Aspects of human fetoplacental vasculogenesis and angiogenesis. I. Molecular regulation. Placenta 2004, 25:103-113.
13. Dehoff R.T. Curvature and the topological properties of interconnected phases. Quantitative Microscopy 1968, 291-325. McGraw-Hill Book Company, New York. R.T. Dehoff, F.N. Rhines (Eds.).
14. Dockery P., Fraher J. The quantification of vascular beds: a stereological approach. Exp. Mol. Pathol. 2007, 82:110-120.
15. Dorph-Petersen K.A., Nyengaard J.R., Gundersen H.J. Tissue shrinkage and unbiased stereological estimation of particle number and size. J. Microsc. 2001, 204:232-246.
16. Eisele J.C., Schaefer I.M., Nyengaard J.R., Post H., Liebetanz D., Brüel A., Mühlfeld C. Effect of voluntary exercise on number and volume of cardiomyocytes and their mitochondria in the mouse left ventricle. Basic Res. Cardiol. 2008, 103:12-21.
17. Fidzianska A., Walczak E., Glinka Z., Religa G., Sobieszczanska-Malek M., Bilinska Z.T. Ultrastructural evidence of myocardial capillary remodeling in peripartum cardiomyopathy. Med. Sci. Monit. 2010, 16:CS62-CS66.
18. Gehr P., Bachofen M., Weibel E.R. The normal human lung: ultrastructure and morphometric estimation of diffusion capacity. Respir. Physiol. 1978, 32:121-140.
19. Gehr P., Mwangi D.K., Ammann A., Maloiy G.M., Taylor C.R., Weibel E.R. Design of the mammalian respiratory system. V. Scaling morphometric pulmonary diffusing capacity to body mass: wild and domestic mammals. Respir. Physiol. 1981, 44:61-86.
20. Gruber C., Nink N., Nikam S., Magdowski G., Kripp G., Voswinckel R., Mühlfeld C. Myocardial remodelling in left ventricular atrophy induced by caloric restriction. J. Anat. 2012, 220:179-185.
21. Gruber C., Kohlstedt K., Loot A.E., Fleming I., Kummer W., Mühlfeld C. Stereological characterization of left ventricular cardiomyocytes, capillaries, and innervation in the nondiabetic, obese mouse. Cardiovasc. Pathol. 2012, (Epub ahead of print).
22. Gundersen H.J.G., Østerby R. Optimizing sampling efficiency of stereological studies in biology: or "Do more less well!". J. Microsc. 1981, 121:65-73.
23. Gundersen H.J.G., Jensen E.B. The efficiency of systematic sampling in stereology and its prediction. J. Microsc. 1987, 147:229-263.
24. Gundersen H.J., Bagger P., Bendtsen T.F., Evans S.M., Korbo L., Marcussen N., Moller A., Nielsen K., Nyengaard J.R., Pakkenbarg B., et al. The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 1988, 96:857-881.
25. Gundersen H.J., Boyce R.W., Nyengaard J.R., Odgaard A. The conneulor: unbiased estimation of connectivity using physical dissectors under projection. Bone 1993, 14:217-222.
26. Gundersen H.J., Jensen E.B., Kieu K., Nielsen J. The efficiency of systematic sampling in stereology - reconsidered. J. Microsc. 1999, 193:199-211.
27. Gundersen H.J. The smooth fractionator. J. Microsc. 2002, 207:191-210.
28. Hansen-Smith F.M. Capillary network patterning during angiogenesis. Clin. Exp. Pharmacol. Physiol. 2000, 27:830-835.
29. Hayat M. Principles and Techniques of Electron Microscopy 2000, Cambridge University Press, Cambridge.
30. Hill J.A., Olson E.N. Cardiac plasticity. N. Engl. J. Med. 2008, 358:1370-1380.
31. Howard C.V., Reed M.G. Unbiased Stereology: Three-Dimensional Measurement in Microscopy 2005, Garland Science/BIOS Scientific, Abingdon. 2nd ed.
32. Hsia C.C., Hyde D.M., Ochs M., Weibel E.R. An official research policy statement of the American Thoracic Society/European Respiratory Society: standards for quantitative assessment of lung structure. Am. J. Respir. Crit. Care Med. 2010, 181:394-418. ATS/ERS Joint Task Force on Quantitative Assessment of Lung Structure.
33. Hyde D.M., Tyler N.K., Plopper C.G. Morphometry of the respiratory tract: avoiding the sampling, size, orientation and reference traps. Toxicol. Pathol. 2007, 35:41-48.
34. Kaufmann P., Mayhew T.M., Charnock-Jones D.S. Aspects of human fetoplacental vasculogenesis and angiogenesis. II. Changes during normal pregnancy. Placenta 2004, 25:114-126.
35. Koyama T., Xie Z., Gao M., Suzuki J., Batra S. Adaptive changes in the capillary network in the left ventricle of rat heart. Jpn. J. Physiol. 1998, 48:229-241.
36. Kroustrup J.P., Gundersen H.J. Sampling problems in a heterogeneous organ: quantitation of relative and total volume of pancreatic islets by light microscopy. J. Microsc. 1983, 132:43-55.
37. Laflamme M.A., Murry C.E. Heart regeneration. Nature 2011, 473:326-335.
38. Li L., Mühlfeld C., Niemann B., Pan R., Li R., Hilfiker-Kleiner D., Chen Y., Rohrbach S. Mitochondrial biogenesis and PGC-1α deacetylation by chronic treadmill exercise: differential response in cardiac and skeletal muscle. Basic Res. Cardiol. 2011, 106:1221-1234.
39. Lojda Z. Studies on dipeptidyl(amino)peptidase IV (glycyl-proline naphthylamidase) II blood vessels. Histochemistry 1979, 59:153-166.
40. Lokmic Z., Mitchell G.M. Visualisation and stereological assessment of blood and lymphatic vessels. Histol. Histopathol. 2011, 26:781-796.
41. Mandelbrot B. How long is the coast of Britain? Statistical self-similarity and fractional dimension. Science 1967, 156:636-638.
42. Mattfeldt T., Krämer K.L., Zeitz R., Mall G. Stereology of myocardial hypertrophy induced by physical exercise. Virchows Arch. Pathol. Anat. 1986, 409:473-484.
43. Mattfeldt T., Mall G., Gharehbaghi H., Möller P. Estimation of surface area and length with the orientator. J. Microsc. 1990, 159:301-317.
44. Mayhew T.M. Taking tissue samples from the placenta: an illustration of principles and strategies. Placenta 2008, 29:1-14.
45. Mayhew, T.M. Estimating oxygen diffusive conductances of gas-exchange systems: a stereological approach illustrated with the human placenta. Ann. Anat., , in this issue. doi:10.1016/j.aanat.2012.08.002.
46. Mayhew T.M., Charnock-Jones D.S., Kaufmann P. Aspects of human fetoplacental vasculogenesis and angiogenesis. III. Changes in complicated pregnancies. Placenta 2004, 25:127-139.
47. Michel R.P., Cruz-Orive L.M. Application of the Cavalieri principle and vertical sections method to lung: estimation of volume and pleural surface area. J. Microsc. 1988, 150:117-136.
48. Mühlfeld C., Nyengaard J.R., Mayhew T.M. A review of state-of-the-art stereology for better quantitative 3D morphology of the heart. Cardiovasc. Pathol. 2010, 19:65-82.
49. Mühlfeld C., Papadakis T., Krasteva G., Nyengaard J.R., Hahn U., Kummer W. An unbiased stereological method for efficiently quantifying the innervation of the heart and other organs based on total length estimations. J. Appl. Physiol. 2010, 108:1402-1409.
50. Mühlfeld C., Weibel E.R., Hahn U., Kummer W., Nyengaard J.R., Ochs M. Is length an appropriate estimator to characterize pulmonary alveolar capillaries? A critical evaluation in the human lung. Anat. Rec. 2010, 293:1270-1275.
51. Nyengaard J.R., Gundersen H.J. The isector: a simple and direct method for generating isotropic, uniform random sections from small specimens. J. Microsc. 1992, 165:427-431.
52. Nyengaard J.R. Number and dimensions of rat glomerular capillaries in normal development and after nephrectomy. Kidney Int. 1993, 43:1049-1057.
53. Nyengaard J.R. Stereological methods and their application in kidney research. J. Am. Soc. Nephrol. 1999, 10:1100-1123.
54. Olivetti G., Anversa P., Loud A.V. Morphometric study of early postnatal development in the left and right ventricular myocardium of the rat. II. Tissue composition, capillary growth, and sarcoplasmic alterations. Circ. Res. 1980, 46:503-512.
55. Schaper J., Meiser E., Stämmler G. Ultrastructural morphometric analysis of myocardium from dogs, rats, hamsters, mice, and from human hearts. Circ. Res. 1985, 56:377-391.
56. Schmidt-Nielsen K., Pennycuik P. Capillary density in mammals in relation to body size and oxygen consumption. Am. J. Physiol. 1961, 200:746-750.
57. Schmiedl A., Schnabel P.A., Richter J., Mall G., Bretschneider H.J. Preservation of cardiac myocytes subjected to different preconditions: a comparative morphometric study of beating, fibrillating, and cardioplegically arrested canine hearts. Anat. Rec. 1993, 235:425-435.
58. Schwanke U., Deussen A., Heusch G., Schipke J.D. Heterogeneity of local myocardial flow and oxidative metabolism. Am. J. Physiol. Heart Circ. Physiol. 2000, 279:H1029-H1035.
59. Sterio D.C. The unbiased estimation of number and sizes of arbitrary particles using the disector. J. Microsc. 1984, 134:127-136.
60. Tang Y., Nyengaard J.R., Andersen J.B., Baandrup U., Gundersen H.J.G. The application of stereological methods for estimating structural parameters in the human heart. Anat. Rec. 2009, 292:1630-1647.
61. Tschanz S.A., Burri P.H., Weibel E.R. A simple tool for stereological assessment of digital images: the STEPanizer. J. Microsc. 2011, 243:47-59.
62. Tschanz, S.A., Schneider, J.P., Knudsen, L. Design-based stereology: planning, volumetry, and sampling are crucial Stepps for a successful study. Ann. Anat., under review.
63. Van Vré E.A., van Beusekorn H.M., Vrints C.J., Bosmans J.M., Bult H., Van der Giessen W.J. Stereology: a simplified and more time-efficient method than planimetry for the quantitative analysis of vascular structures in different models of intimal thickening. Cardiovasc. Pathol. 2007, 16:43-50.
64. Vink A., Schoneveld A.H., Poppen M., de Kleijn D.P., Borst C., Pasterkamp G. Morphometric and immunohistochemical characterization of the intimal layer throughout the arterial system of elderly humans. J. Anat. 2002, 200:97-103.
65. Warley A., Powell J.M., Skepper J.N. Capillary surface area is reduced and tissue thickness from capillaries to myocytes is increased in the left ventricle of streptozotocin-diabetic rats. Diabetologia 1995, 38:413-421.
66. Weibel E.R. Stereological Methods. Practical Methods for Biological Morphometry 1979, vol. 1. Academic Press, New York.
67. Weibel E.R. Stereological Methods. Theoretical Foundations 1980, vol. 2. Academic Press, New York.
68. Weibel E.R., Gomez D.M. Architecture of the human lung. Use of quantitative methods establishes fundamental relations between size and number of lung structures. Science 1962, 137:577-585.
69. Wiest G., Gharehbaghi H., Amann K., Simon T., Mattfeldt T., Mall G. Physiological growth of arteries in the rat heart parallels the growth of capillaries, but not of myocytes. J. Mol. Cell. Cardiol. 1992, 24:1423-1431.
70. Wulfsohn D., Nyengaard J.R., Tang Y. Postnatal growth of cardiomyocytes in the left ventricle of the rat. Anat. Rec. A: Discov. Mol. Cell. Evol. Biol. 2004, 277:236-247.
71. Zachary I., Morgan R.D. Therapeutic angiogenesis for cardiovascular disease: biological context, challenges, prospects. Heart 2011, 97:181-189.
72. Zulli A., Lau E., Wijaya B.P., Jin X., Sutarga K., Schwartz G.D., Learmont J., Wookey P.J., Zinellu A., Carru C., Hare D.L. High dietary taurine reduces apoptosis and atherosclerosis in the left main coronary artery: association with reduced CCAAT/enhancer binding protein homologous protein and total plasma homocysteine but not lipidemia. Hypertension 2009, 53:1017-1022.